Inactivation Effect of Thymoquinone on Alicyclobacillus acidoterrestris Vegetative Cells, Spores, and Biofilms

Alicyclobacillus acidoterrestris (A. acidoterrestris), a spore-forming bacterium, has become a main challenge and concern for the juices and acid beverage industry across the world due to its thermo-acidophilic characteristic. Thymoquinone (TQ) is one of the active components derived from Nigella sativa seeds. The objective of this study was to investigate antibacterial activity and associated molecular mechanism of TQ against A. acidoterrestris vegetative cells, and to evaluate effects of TQ on A. acidoterrestris spores and biofilms formed on polystyrene and stainless steel surfaces. Minimum inhibitory concentrations of TQ against five tested A. acidoterrestris strains ranged from 32 to 64 μg/mL. TQ could destroy bacterial cell morphology and membrane integrity in a concentration-dependent manner. Field-emission scanning electron microscopy observation showed that TQ caused abnormal morphology of spores and thus exerted a killing effect on spores. Moreover, TQ was effective in inactivating and removing A. acidoterrestris mature biofilms. These findings indicated that TQ is promising as a new alternative to control A. acidoterrestris and thereby reduce associated contamination and deterioration in the juice and acid beverage industry.

[1]  D. Maiti,et al.  Attenuation of Pseudomonas aeruginosa biofilm by thymoquinone: an individual and combinatorial study with tetrazine-capped silver nanoparticles and tryptophan , 2021, Folia Microbiologica.

[2]  Lina Wu,et al.  Inhibition of Biofilm Formation and Related Gene Expression of Listeria monocytogenes in Response to Four Natural Antimicrobial Compounds and Sodium Hypochlorite , 2021, Frontiers in Microbiology.

[3]  Du Guo,et al.  Inactivation Efficacy of 405 nm LED Against Cronobacter sakazakii Biofilm , 2020, Frontiers in Microbiology.

[4]  D. Laskowski,et al.  Clove Oil (Syzygium aromaticum L.) Activity against Alicyclobacillus acidoterrestris Biofilm on Technical Surfaces , 2020, Molecules.

[5]  Daoying Wang,et al.  Antibacterial activity and action mode of chlorogenic acid against Salmonella Enteritidis, a foodborne pathogen in chilled fresh chicken , 2020, World Journal of Microbiology and Biotechnology.

[6]  S. Pornpukdeewattana,et al.  Alicyclobacillus spoilage and control - a review , 2020, Critical reviews in food science and nutrition.

[7]  X. Xia,et al.  Thymoquinone Inhibits Biofilm Formation and Attachment-Invasion in Host Cells of Vibrio parahaemolyticus. , 2019, Foodborne pathogens and disease.

[8]  C. Nakamura,et al.  Effect of ultraviolet (UV-C) radiation on spores and biofilms of Alicyclobacillus spp. in industrialized orange juice. , 2019, International journal of food microbiology.

[9]  Hao Wu,et al.  Transcriptomic Analysis of the Molecular Mechanisms Underlying the Antibacterial Activity of IONPs@pDA-Nisin Composites toward Alicyclobacillus acidoterrestris. , 2019, ACS applied materials & interfaces.

[10]  J. Ryu,et al.  Inhibition of Listeria monocytogenes using biofilms of non-pathogenic soil bacteria (Streptomyces spp.) on stainless steel under desiccated condition. , 2019, Food microbiology.

[11]  Yahong Yuan,et al.  Antibacterial activity and mechanism of thymol against Alicyclobacillus acidoterrestris vegetative cells and spores , 2019, LWT.

[12]  Yuyang Sun,et al.  Antibacterial and anti-biofilm activities of peppermint essential oil against Staphylococcus aureus , 2019, LWT.

[13]  Yahong Yuan,et al.  Antibacterial activity and mechanism of cinnamic acid and chlorogenic acid againstAlicyclobacillus acidoterrestrisvegetative cells in apple juice , 2018, International Journal of Food Science & Technology.

[14]  C. Nakamura,et al.  Biofilm‐forming ability of Alicyclobacillus spp. isolates from orange juice concentrate processing plant , 2018 .

[15]  Chunling Zhang,et al.  Effect of Coenzyme Q0 on biofilm formation and attachment-invasion efficiency of Listeria monocytogenes , 2018, Food Control.

[16]  C. Nakamura,et al.  Piperaceae extracts for controlling Alicyclobacillus acidoterrestris growth in commercial orange juice , 2018, Industrial Crops and Products.

[17]  H. Shaterzadeh-Yazdi,et al.  An Overview of Hepatoprotective Effects of Thymoquinone. , 2018, Recent patents on food, nutrition & agriculture.

[18]  H. Tag,et al.  Black Seed Thymoquinone Improved Insulin Secretion, Hepatic Glycogen Storage, and Oxidative Stress in Streptozotocin-Induced Diabetic Male Wistar Rats , 2018, Oxidative medicine and cellular longevity.

[19]  Chunhong Yan,et al.  Thymoquinone Inhibits Virulence Related Traits of Cronobacter sakazakii ATCC 29544 and Has Anti-biofilm Formation Potential , 2017, Front. Microbiol..

[20]  Yahong Yuan,et al.  Activity of paracin C from lactic acid bacteria against Alicyclobacillus in apple juice: Application of a novelty bacteriocin , 2017 .

[21]  X. Xia,et al.  Antimicrobial Activity of Punicalagin Against Staphylococcus aureus and Its Effect on Biofilm Formation. , 2017, Foodborne pathogens and disease.

[22]  Evelyn,et al.  High pressure processing pretreatment enhanced the thermosonication inactivation of Alicyclobacillus acidoterrestris spores in orange juice , 2016 .

[23]  C. Shi,et al.  Effect of tea tree oil on Staphylococcus aureus growth and enterotoxin production , 2016 .

[24]  A. Klančnik,et al.  Control of Alicyclobacillus spp. vegetative cells and spores in apple juice with rosemary extracts , 2016 .

[25]  Yutang Wang,et al.  Precursors and metabolic pathway for guaiacol production by Alicyclobacillus acidoterrestris. , 2015, International journal of food microbiology.

[26]  Çelenk Molva,et al.  Evaluation of bioactivity of pomegranate fruit extract against Alicyclobacillus acidoterrestris DSM 3922 vegetative cells and spores in apple juice , 2015 .

[27]  V. Gekas,et al.  Alicyclobacillus in the Fruit Juice Industry: Spoilage, Detection, and Prevention/Control , 2015 .

[28]  H. Hosseinzadeh,et al.  Iranian Journal of Basic Medical Sciences Black Cumin (nigella Sativa) and Its Constituent (thymoquinone): a Review on Antimicrobial Effects , 2022 .

[29]  M. Shemesh,et al.  External pH is a cue for the behavioral switch that determines surface motility and biofilm formation of Alicyclobacillus acidoterrestris. , 2014, Journal of food protection.

[30]  D. Hoskin,et al.  Thymoquinone, A Bioactive Component of Black Caraway Seeds, Causes G1 Phase Cell Cycle Arrest and Apoptosis in Triple-Negative Breast Cancer Cells with Mutant p53 , 2014, Nutrition and cancer.

[31]  V. Antolinos,et al.  Combined effect of natural antimicrobials and thermal treatments on Alicyclobacillus acidoterrestris spores , 2014 .

[32]  Jing Yang,et al.  Thymoquinone inhibits proliferation and invasion of human nonsmall-cell lung cancer cells via ERK pathway , 2014, Tumor Biology.

[33]  A. Navarro,et al.  Chemicals and lemon essential oil effect on Alicyclobacillus acidoterrestris viability , 2013, Brazilian journal of microbiology : [publication of the Brazilian Society for Microbiology].

[34]  C. Nakamura,et al.  Resistance of Alicyclobacillus acidoterrestris spores and biofilm to industrial sanitizers. , 2013, Journal of food protection.

[35]  Yahong Yuan,et al.  Alicyclobacillus Contamination in the Production Line of Kiwi Products in China , 2013, PloS one.

[36]  A. A. Tribst,et al.  Thermal Inactivation of Alicyclobacillus acidoterrestris in a Model Food , 2011 .

[37]  R. Witthuhn,et al.  Alicyclobacillus spoilage and isolation--a review. , 2011, Food microbiology.

[38]  L. Mahran,et al.  Anti-asthmatic and Anti-allergic effects of Thymoquinone on Airway-Induced Hypersensitivity in Experimental Animals , 2011 .

[39]  C. Yeo,et al.  Anti-inflammatory effects of the Nigella sativa seed extract, thymoquinone, in pancreatic cancer cells. , 2009, HPB : the official journal of the International Hepato Pancreato Biliary Association.

[40]  A. Basson,et al.  Evaluation of Adherence, Hydrophobicity, Aggregation, and Biofilm Development of Flavobacterium johnsoniae-Like Isolates , 2007, Microbial Ecology.

[41]  K. Goto.  Thermophilic, Acidophilic Spore-forming Bacilli, Alicyclobacillus, and Spoilage of Acidic Beverages , 2006 .

[42]  Xiaosong Hu,et al.  Isolation and characterization of thermo-acidophilic endospore-forming bacteria from the concentrated apple juice-processing environment. , 2006, Food microbiology.

[43]  V. Gökmen,et al.  Formation of guaiacol from vanillin by Alicyclobacillus acidoterrestris in apple juice: a model study , 2005 .